Seasonal sequences of bioluminescense in waters around Woods Hole were measured in 1961 to 1963. Peak activities occurred in October-November (once) and in April-May (twice). Bioluminescense at night is usually quantitatively greater than during the day. Greater differences during summer correlate with the seasonal maximum in solar radiation...

Laird, J. C.

Yentsch, Charles S.

English

Yale University

      P.O. BOX 208118 | NEW HAVEN CT 06520-8118 USA | PEABODY.YALE. EDU   JOURNAL OF MARINE RESEARCH The Journal of Marine Research, one of the oldest journals in American marine science, published important peer-reviewed original research on a broad array of topics in physical, biological, and chemical oceanography vital to the academic oceanographic community in the long and rich tradition of the Sears Foundation for Marine Research at Yale University.  An archive of all issues from 1937 to 2021 (Volume 1–79) are available through EliScholar,  a digital platform for scholarly publishing provided by Yale University Library at  https://elischolar.library.yale.edu/.  Requests for permission to clear rights for use of this content should be directed to the authors, their estates, or other representatives. The Journal of Marine Research has no contact information beyond the affiliations listed in the published articles. We ask that you provide attribution to the Journal of Marine Research.  Yale University provides access to these materials for educational and research purposes only. Copyright or other proprietary rights to content contained in this document may be held by individuals or entities other than, or in addition to, Yale University. You are solely responsible for determining the ownership of the copyright, and for obtaining permission for your intended use. Yale University makes no warranty that your distribution, reproduction, or other use of these materials will not infringe the rights of third parties.  This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License. https://creativecommons.org/licenses/by-nc-sa/4.0/   Seasonal Sequence of Bioluminescence and the Occurrence of Endogenous Rhythms tn Oceanic Waters off Woods Hole, Massachusetts' Charles S. Yentsch and J. C. Laird Physical Oceanographic Laboratory N ova University Fort Lauderdale, Florida ABSTRACT Seasonal sequences of bioluminescense in waters around Woods Hole were measured in 1961 to 1963. Peak activities occurred in October-November (once) and in April-May (twice). Bioluminescense at night is usually quantitatively greater than during the day. Greater differences during summer correlate with the seasonal maximum in solar radiation. Endogenous "biological clock" rhythms that are apparent during summer months disappear when water temperatures fall below approximately 14°C. Interrelationships between exogen-ous and endogenous rhythms are discussed. Introduction. In the oceans' surface waters, the capacity for bioluminescence is at a maximum about midnight and at a minimum during midday (Backus et al. 1961 ). Varying explanations for these diurnal changes have been offered. In the open ocean, the diurnal pattern has been observed throughout the euphotic zone, with day-to-night differences least near the base of the euphotic zone (Yentsch et al. 1964); from these observations it was concluded that diurnal changes in light intensity directly control the intensity of biolum-inescence through the processes of photoinhibition and photoenhancement. Kelly and Katona ( 1966) observed, in natural populations from Woods Hole waters, that the sensitivity of bioluminescence to light varied diurnally, con-trolled by an endogenous 'biological clock' rhythm. Soli ( 1966) observed that bioluminescent dinoflagellates in shallow tropical waters migrate downward during the day and congregate near the surface at night, thereby partially initiating a diurnal pattern. r. Contribution 2065 from the Woods Hole Oceanographic Institution. Accepted for publication and submitted to press 3 February 1968. This work was supported by National Science Foundation contracts GB 5456 and GB443 r with the Woods Hole Oceanographic Institution. The authors acknowledge the assistance of A. S. Wing. 127 F igure r. 700 600 20' ' t I<, 1s•~ 500 " I!; 10 • 4 00 'l I<, __, "' ,. 300 I!; " __, "' o· 200 -5' 100 70,000 60,000 sopoo ii! c,j 40,000 ... ... :J: 30.000 "' " 20,000 10,000 A ' --\ : ( 7,90 1) / / ·""- I\. ~-, v · / ,,_.,-..,,,./ "/"'-. _ _,,,,-· ~-, ____ , .r\/ . "'-,_.J TE MPERATURE SOLAR RAOIATION,lN LANGLE YS!C:ay-l) SALINITY (•4•1 33.0 ,O.Q \ I ~--------------~11~"-·-··----------------------1 ---.: -- ---- - - - ---- ---- ' 170 71 7000 700 j\-\ - r\ / 0 " 1961 j . ii i \ · j . I I . I . I . \ I / . I Iii \ / I i -I \ t\ . i t .. . . I '-J /V NIGHT OAY RATIO \-o __ _ ... M (963 M 6000 600 5000 500 \::! 4000 ""'( 400 c'; N 0 D 3000 300 2000 200 1000 IOO (A) Seasonal sequence of temperature, sal in ity, and solar radiation at Woods Hole, M assachusetts (weekly averages). (B) Seasonal sequence of nighttime and daytime bioluminescence and the ratio of nighttime-to-daytime counts. The data are weekly averages of daily counts occurring at 1100, 1200, 1300 h (daytime) and at 2300, 2 4 00, 0100 h (nighttime). Iv 00 I 968] Yentsch and Laird: Bioluminescence and Endogenous Rhythms I 29 As part of a continuing study on bioluminescence in natural populations, seasonal measurements of the capacity for bioluminescence (stimulated) were made in the surface waters off Woods Hole. These measurements were made to investigate: (i) whether a relationship exists between the ratio of night-to-day bioluminescence and to seasonal change in solar radiation, assuming that diurnal changes in light intensity directly control bioluminescence; (ii) whether endogenous rhythm occurs persistently in natural populations, as-suming that exogenous rhythm (diurnal change) is present throughout the year and is somehow under the control of the endogenous rhythm. Methods. The apparatus used for the measurements of bioluminescence was basically the same as that described by Backus et al. (1961). Seawater was pumped through a cuvette at 24 1/min. The cuvette was viewed by a photo-multiplier, RCA 6655, with an S-1 I response. The cuvette and tube were in a light-tight container. Bioluminescence was stimulated by the turbulent flow through the cuvette. Individual flashes were recorded as counts and were tallied. To test for endogenous rhythms, 100 l of Vineyard Sound surface water were held at ambient temperature in a darkened container and period-ically pumped through the cuvette and back into the container. Every hour a time switch started the pump and then stopped it after it had run for one minute. Results. The waters around Woods Hole vary seasonally over wide ranges of water temperature and solar radiation, with slight changes in salinity (Fig. I a). The minimum solar radiation, about 100 langleys per day, occurs in December, and the maximum, around 6 50 langleys per day, occurs in July. Freezing water temperatures (- 2.5°C) occur in February and near-tropical temperatures ( 24.0°C) occur in July and August. The mean weekly bioluminescence at midday and midnight was measured for 20 months (Fig. I b). The variation is greatest in the nighttime counts. The maximum bioluminescence occurred during fall and early winter or in early spring, whereas the minimum occurred in late winter, summer, and early fall. These pulses of bioluminescence correlate roughly with the seasonal sequence of phytoplankton in waters off Woods Hole (Fish 1952). A massive amount of bioluminescence, nighttime maximum, occurred during the fall of 1961. This occurred with a large bloom of diatoms and dinoflagellates (Conover, unpublished). The ratio of day and night counts was not constant throughout the year; the ratios were smaller during the winter. Frequently nighttime counts were 10 to 100 times greater than daytime counts (Fig. I b). During a few days in winter, when the amount of daylight was low, nighttime counts were lower than the daytime counts. In summer, nighttime counts were approximately 250 to 700 times greater than daytime counts (Fig. 1 b). The seasonal trend 300 100 200 <:,j i-..: \.) 100 . . .... HOURS Figure 2. Stimulated bioluminescense of a natural populat ion in total darkness; started October 28, 196 5; water temperature 14° C . .. .. .. .. . . . . . . . . ...... . . . . . . . . . . . . . . . . . . . . . .. . .. 300 200 100 200 100 L..J....L..I....LL-'--'.-'--'-'--'2W3'-45'-'-'-'--'-'--'--'--'--'JIJl '-4 '-5 '-'--'--'--'-'--'--'-'--'2J34~5'-'-'-'--'--'--'-'--'--'JIJl 4~5:-'-'-'-'-'--'-'--'--'-2-:'-.3:-'4J5-'--''-'-'-'--'-'--'--'--'-I JI 4J5-'--'L...I....L..I....LL-Ll..J.23.J.4_j5...J_LLLL.L.L..L..l..J.l_jl 4-'5-'-LJ O HOURS Figure 3. Stimulated bioluminescense of a natural population in total darkness; started December , 6, , 96 5; water temperature 5.5°C. .... w 0 1968] Yentsch and Laird: Bioluminescence and Endogenous Rhythms 131 in the ratio of night to day is roughly correlated with the seasonal change in light intensity and water temperature. However, large weekly variations in ratio and radiation suggest that the ratio is influenced primarily by radiation. In the experiments to detect endogenous rhythm, darkened natural popula-tions always produced an initial increase in bioluminescence. If a sharp decline and a second increase were not observed, endogenous rhythm was considered to be absent. A persistent endogenous rhythm with a 23-to-24-hour period was observed during October (Fig. 2). With time, rhythmic pulses became less definite, with a decline in the maximum bioluminescence. Fig. 3 is an example of a record where no conspicuous rhythm was observed; in this case, following an initial increase, bioluminescence declined more rapidly during the first Io hours than during the remainder of the experiment. Some experiments, par-ticularly in winter, showed a slower decline in the bioluminescence during darkness. Endogenous rhythm was undetected from November to early June, whereas exogenous diurnal rhythm persisted throughout the year (Table I); endogenous rhythm appeared repeatedly during August when the water tem-perature was the highest. Discussion. The endogenous rhythm of bioluminescence observed in these natural populations appears to be similar to endogenous rhythm studied in laboratory cultures of Gonyaulax polyedra; in such cultures (Sweeney and Hastings 1957) and in natural populations (Kelly and Katona 1966), studies of the sensitivity of bioluminescence to light show that photoinhibition is at a maximum from morning through midday and at a minimum during the night. Endogenous regulation of the sensitivity of bioluminescence to light intensity could control the diurnal bioluminescence. But, it is difficult to argue for any endogenous control when the seasonal persistence of endogenous rhythm cannot be established (Table I) while the diurnal exogenous rhythm is a persistent year-long feature of natural populations. Endogenous rhythms are not present in all dinofl.agellates (Hastings 1959); the seasonal change in species in natural waters could explain the variable appearance of endogenous rhythms. Even if organisms with 'biological clocks' are present, it would be unlikely that endo-genous rhythms could be observed when water temperatures are much below I 2°c. In G. polyedra the endogenous rhythm disappears at I 1.4 °C; how-ever, the organisms are still viable and bioluminescent at that temperature (Hastings and Sweeney 1957). In both cultures and natural populations of dinofl.agellates, the capacity for bioluminescence in darkness increases and reaches a maximum after a few hours. In G. polyedra the maximum production of the luminescent substrate luciferin occurs in darkness (Bode et al. 1963). Soli (1966) has emphasized that this reduced substance is likely to occur in maximum production in a low oxygen-tension environment. In cultured marine phytoplankton, the capacity for oxygen evolution by photosynthesis is enhanced by short residence in darkness 132 'Journal of M arine Research [ 26,2 Table I. Seasonal appearance of rhythms of bioluminescence in waters off Woods Hole. Plus indicates rhythm, minus indicates absence. Date Midday (OC) VIII /7/65 . ... . . .. . . 21 VIII / 12/65 . ..... . .. 21 VIII /30/65 . .... . . . . 20 IX /8/65 .. . .... .. ... 18 IX /29/65 . .. ... . .. . . 16 X/28/65 . . .. . . . .. ... 14 XI /5/65 . ... .... . . .. 8 XI /12/65 .. ... .. ... . 7.2 X II / 16/65 .. ... . .. . . 5.5 I/3/66 .......... . . . 2.5 I / 17/66 . . . . .. . ..... 1.8 II /5/66 ...... . . . . . . 0.5 II / 15/66 ......... .. 0 III /4/66 . . . . . . . . . . . 0.5 III /7/66 . . . . . . . . . . . 0 III/18 /66 .... ... . . . 1.8 III /25/66 . .. . ... .. . 3.9 IV /5/66 . . .. . . . .. . . . 6.0 IV / 18/66 . . . ....... . 7.1 IV /25/66 ... . ... ... . 7.8 V/3/66 ... .. .... . . .. 8.0 Vf17/66 . . .... .. . .. . 10.0 V/20/66 .. . . ....... . IO.I V/26/66 ..... . . . . . .. 13.2 VI /3/66 .. . ......... 14.8 VI /25/66 ... . . . .. . .. 17.9 VII /7/66 . .. . ....... 20.0 VIII /8/66 .. .. . . .. . . 21.0 IX/9/66 .. . .... .. . . . 22.5 Exogenous rhythm temp. (Night > Day) + + + + + + + + + + + + + + + + + + + + + + + + + + + + + Endogenous rhythm + + + + + + + + (Yentsch and Reichert 1963). It is beli eved that this results from a more rapid production of enzymes in darkness than in li ght. In similar fashion, luciferin concentrations could be expected to increase in the low oxygen-tension environment created by darkness. With more li ght, the synthesis of luciferin would be rapidly retarded because of highly effi cient production of oxygen by photosynthesis. Therefore, day-to-night changes in bioluminescence could be the result of variations in substrate producti on, regulated by oxygen tension, which is controlled by photosynthesis and respiration. Considering the variety of bioluminescent organisms in the oceans, gener-alizations about the influence of diurnal migrati ons upon diurnal biolumin-escence are difficult. In shall ow tropical waters, diurnal migrations appear to be very important. In open waters having a deep euphotic zone ( > 50 m), it is diffi cult to imagine that the magnitude of vertical migration can change the pattern of bioluminescence in the uniform manner observed by Yentsch et al. Yentsch and Laird: Bioluminescence and Endogenous Rhythms 133 (1964). In contrast to Soli's (1966) observations in a shallow tropical lagoon, the intense tidal action around Woods Hole would tend to obscure most vertical stratification of organisms resulting from migratory patterns. More-over, recordings of bioluminescent Rashes in the euphotic zone show that amplitudes of Rash are much smaller in daylight than in darkness (Clarke and Kelly 1965), thus demonstrating that the organisms present during daylight have a reduced capability to bioluminesce. The data shown in Fig. 1 b reaffirm the importance of light intensity in controlling the magnitude of diurnal change. The model that considers photo-inhibition and photoenhancement (Yentsch et al. 1964) is believed to offer the only practical interpretation of diurnal changes in bioluminescence in natural dinoRagellate populations of the open ocean. REFERENCES BACKUS, R. H ., C. S. YENTSCH, and A. S. WING 1961. Bioluminescense in the surface waters of the sea. Nature, London, I92 (4802): 518-521. BooE, V. C., R . DESA, and J. W. HASTINGS 1963. Daily rhy thm of luciferin activity in Gonyaulax po!yedra. Science, I4I: 913-915. CLARKE, G. L., and M. G. KELLY 1965. Measurements of diurnal changes in bioluminescence from the sea surface to 2,000 meters using a new photometric device. Limnol. Oceanogr., IO, Suppl.: R 54-R 66. FISH, C. J. 1952. Seasonal distribution of the plankton of the vVoods Hole region. Bull. U.S.Bur. Fish., 4I; 179 pp. HASTINGS,]. W . 1959. Unicellular clocks. Ann. Rev. Microbial., IJ: 297-312. HASTINGS, J. W., and B. M. SWEENEY 1957. On the mechanism of temperature independence in a biological clock. Proc. nat. Acad. Sci., 43: 804-811. KELLY, M . G., and S. KATONA 1966. An endogenous diurnal rhythm of bioluminescence in a natural population of dino-fiagellates. Biol. Bull. Woods Hole, IJI: II 5-126. Sou, G. 1966. Bioluminescent cycle of photosynthetic dinofiagellates. Limnol. Oceanogr., II (3): 355-363. SWEENEY, B. M., and J. W. HASTINGS 1957. Characteristics of the diurnal rhythm of luminescence in Gonyaulax po!yedra. J. cell. comp. Physiol., 49 (1): II5-128. YENTSCH, C. S., R. H . BACKUS, and A. S. WING 1964. Factors affecting the vertical distribution of bioluminescense in the euphotic zone. Limnol. Oceanogr., 9 (4): 519-524. YENTSCH, C. S., and C. A. REICHERT 1963. The effects of prolonged darkness on photosynthesis, respiration, and chlorophyll in the marine flagellate, Dunaliella euchlora. Limnol. Oceanogr., 8 (3): 338-342. 

Seasonal sequence of bioluminescence and the occurrence of endogenous rhythms in oceanic waters off Woods Hole, Massachusetts

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Seasonal sequence of bioluminescence and the occurrence of endogenous rhythms in oceanic waters off Woods Hole, Massachusetts

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